Current status and implications of autoimmune antiphospholipid antibodies in relation to thrombotic disease

Journal of Thrombosis and Haemostasis

Volumn 1, Issue 5, 2003, Pages 931-942

  Arnout, J ^a   Vermylen, J ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Antiphospholipid antibodies; Lupus anticoagulant; Thrombosis

Indexed keywords

EID: 0141517177     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1046/j.1538-7836.2003.00125.x     Document Type: Review

References (115)

1. Conley CL, Hartmann RC. A hemorrhagic disorder caused by circulating anticoagulants in patients with disseminated lupus erythematosus. J Clin Invest 1952; 31: 621-2.
2. Moore JE, Mohr CF. Biologically false positive serological tests for syphilis. Type, incidence and cause. J Am Med Assoc 1952; 150: 467-73.
3. Frick PG. Acquired circulating anticoagulants in systemic 'collagen disease'. Autoimmune thromboplastin deficiency. Blood 1955; 10: 691-706.
4. Lechner K. A new type of coagulation inhibitor. Thromb Diath Haemorrh 1969; 21: 482-99.
5. Bowie EJW, Thompson JH Jr, Pascuzzi CA, Owen CA Jr. Thrombosis in systemic lupus erythematosus despite circulating anticoagulants. J Lab Clin Med 1963; 62: 416-30.
6. Feinstein DI, Rapaport SI. Acquired inhibitors of blood coagulation. Prog Hemost Thromb 1972; 1: 75-95.
7. Nilsson IM, Astedt B, Hedner U, Berezin D. Intrauterine death and circulating anticoagulant ('antithromboplastin'). Acta Med Scand 1975; 197: 153-9.
8. Soulier JP, Boffa MC. Avortements a' répé, thromboses et anticoagulant circulant antithromboplastine. Trois observations. Nouvelle Presse Médicale 1980; 9: 859-64.
9. Carreras LO, Defreyn G, Machin SJ, Vermylen J, Deman R, Spitz B, Van Assche A. Arterial thrombosis, intrauterine death and 'lupus' anticoagulant: detection of immunoglobulin interfering with prostacyclin formation. Lancet 1981; i: 244-6.
10. De Wolf F, Carreras LO, Moerman P, Vermylen J, Van Assche A, Renaer M. Decidual vasculopathy and extensive placental infarction in a patient with repeated thromboembolic accidents, recurrent fetal loss and a lupus anticoagulant. Am J Obstetrics Gynecol 1982; 142: 829-34.
11. Harris EN, Gharavi AE, Boey ML, Patel BM, Mackworth-Young CG, Loizou S, Hughes GRV. Anticardiolipin antibodies: detection by radioimmunoassay and association with thrombosis in systemic lupus erythematosus. Lancet 1983; ii: 1211-4.
12. Hughes GRV. The anticardiolipin syndrome. Clin Exp Rheumatol 1985; 3: 285-6.
13. Hughes GRV, Harris EN, Gharavi AE. The anticardiolipin syndrome. J Rheumatol 1986; 13: 486-9.
14. McNeil HP, Simpson RJ, Chesterman CN, Krilis SA. Anti-phospholipid antibodies are directed against a complex antigen that includes a lipid-binding inhibitor of coagulation: beta-2-glycoprotein I (apolipoprotein H). Proc Natl Acad Sci USA 1990; 87: 4120-4.
15. Galli M, Comfurius P, Maassen C, Hemker HC, de Baets MH, van Breda-Vriesman PJC, Barbui T, Zwaal RFA, Bevers EM. Anticardiolipin antibodies (ACA) directed not to cardiolipin but to a plasma protein cofactor. Lancet 1990; 335: 1544-7.
16. Matsuura E, Igarashi Y, Fujimoto M, Ichikawa K, Koike T. Anticardiolipin cofactor(s) and differential diagnosis of autoimmune disease. Lancet 1990; 336: 177-8.
17. Loeliger A. Prothrombin as co-factor of the circulating anticoagulant in systemic lupus erythematosus? Thromb Diath Haemorrh 1959; 3: 273-6.
18. Bevers EM, Galli M, Barbui T, Comfurius P, Zwaal RF. Lupus anticoagulant IgG's (LA) are not directed to phospholipids only, but to a complex of lipid-bound human prothrombin. Thromb Haemost 1991; 66: 629-32.
19. Roubey RA. Update on antiphospholipid antibodies. Curr Opin Rheumatol 2000; 12: 374-8.
20. Arnout J, Wittevrongel C, Vermylen J. Phospholipid-binding proteins and the antiphospholipid syndrome: a role for complement factor H? Thromb Haemost 1997: Suppl. 1; 1.
21. Wilson WA, Gharavi AE, Koike T, Lockshin MD, Branch DW, Piette JC, Brey R, Derksen R, Harris EN, Hughes GR, Triplett DA, Khamashta MA. International consensus statement on preliminary classification criteria for definite antiphospholipid syndrome: report of an international workshop. Arthritis Rheum 1999; 42: 1309-11.
22. Caronti B, Calderaro C, Alessandri C, Conti F, Tinghino R, Palladini G, Valesini G. Beta2-glycoprotein I (beta2-GPI) mRNA is expressed by several cell types involved in anti-phospholipid syndrome-related tissue damage. Clin Exp Immunol 1999; 115: 214-9.
23. Lozier J, Takahashi N, Putnam FW. Complete amino acid sequence of human plasma beta 2-glycoprotein I. Proc Natl Acad Sci USA 1984; 81: 3640-4.
24. Steinkasserer A, Barlow PN, Willis AC, Kertesz Z, Campbell ID, Sim RB, Norman DG. Activity, disulphide mapping and structural modelling of the fifth domain of human beta 2-glycoprotein I. FEBS Lett 1992; 313: 193-7.
25. Bouma B, de Groot PG, van den Elsen JM, Ravelli RB, Schouten A, Simmelink MJ, Derksen RH, Kroon J, Gros P. Adhesion mechanism of human beta(2)-glycoprotein I to phospholipids based on its crystal structure. EMBO J 1999; 18: 5166-74.
26. Schwarzenbacher R, Zeth K, Diederichs K, Gries A, Kostner GM, Laggner P, Prassl R. Crystal structure of human beta2-glycoprotein I. Implications for phospholipid binding and the antiphospholipid syndrome. EMBO J 1999; 18: 6228-39.
27. Ohkura N, Hagihara Y, Yoshimura T, Goto Y, Kato H. Plasmin can reduce the function of human beta2 glycoprotein I by cleaving domain V into a nicked form. Blood 1998; 91: 4173-9.
28. Mann K. Prothrombin and thrombin. In: Hemostasis and Thrombosis: Basic Principles and Clinical Practice. Colman, RW, Hirsh, J, Marder, VJ, Salzman, EW, eds. Philadelphia: J.B. Lippincott 1994: 184-99.
29. Davidson A, Diamond B. Autoimmune diseases. N Engl J Med 2001; 345: 340-50.
30. Dighiero G, Rose NR. Critical self-epitopes are key to the understanding of self-tolerance and autoimmunity. Immunol Today 1999; 20: 423-8.
31. Goldrath AW, Bevan MJ. Selecting and maintaining a diverse T-cell repertoire. Nature 1999; 402: 255-62.
32. Gu H, Tarlinton D, Muller W. Rajewski K, Forster I. Most peripheral B cells in mice are ligand selected. J Exp Med 1991; 173: 1357-71.
33. Coutinho A, Kazatchkine MD, Avrameas S. Natural autoantibodies. Curr Opin Immunol 1995; 7: 812-8.
34. Hayakawa K, Asano M, Shinton SA, Gui M, Allman D, Stewart CL, Silver J, Hardy RR. Positive selection of natural autoreactive B cells. Science 1999; 285: 113-6.
35. Avameas S. Natural autoantibodies: from 'horror autotoxicus' to 'gnothi seauton'. Immunol Today 1991; 12: 154-9.
36. Gilles JG, Saint-Remy JMR. Healthy subjects produce both anti-factor VIII and specific antiidiotypic antibodies. J Clin Invest 1994; 94: 1496-505.
37. Kra-Oz Z, Lorber M, Shoenfeld Y, Scharff Y. Inhibitor(s) of natural anti-cardiolipin autoantibodies. Clin Exp Immunol 1993; 93: 265-8.
38. Goodnow CC. Pathways for self-tolerance and the treatment of autoimmune diseases. Lancet 2001; 357: 2115-21.
39. Male C, Lechner K, Eichinger S, Kyrle PA, Kapiotis S,Wank H, Kaider A, Pabinger I. Clinical significance of lupus anticoagulants in children. J Pediatr 1999; 134: 199-205.
40. Blank M, Krause I, Fridkin M, Keller N, Kopolovic J, Goldberg I, Tobar A, Shoenfeld Y. Bacterial induction of autoantibodies to beta2-glycoprotein-I accounts for the infectious etiology of antiphospholipid syndrome. J Clin Invest 2002; 109: 797-804.
41. Gharavi AE, Pierangeli SS, Espinola RG, Liu X, Colden-Stanfield M, Harris EN. Antiphospholipid antibodies induced in mice by immunization with a cytomegalovirus-derived peptide cause thrombosis and activation of endothelial cells in vivo. Arthritis Rheum 2002; 46: 545-52.
42. Male C, Lechner K, Speiser W, Pabinger I. Transient lupus anticoagulants in children: stepwise disappearance of diagnostic features. Thromb Haemost 2000; 83: 174-5.
43. Thiagarajan P, Shapiro SS, De Marco L. Monoclonal immunoglobulin M coagulation inhibitor with phospholipid specificity. Mechanism of lupus anticoagulant. J Clin Invest 1980; 66: 397-405.
44. 2-glycoprotein I binding to phospholipid membranes. Thromb Haemost 1998; 80: 610-4.
45. 2-glycoprotein I complexes to lipid membranes. Biochemistry 1996; 35: 13833-42.
46. 2GPI binding to phospholipids. J Clin Invest 1997; 99: 2260-8.
47. Arnout J, Wittevrongel C, Vanrusselt M, Hoylaerts M, Vermylen J. Beta-2-glycoprotein I dependent lupus anticoagulants form stable bivalent antibody-beta-2-glycoprotein I complexes on phospholipid surfaces. Thromb Haemost 1998; 79: 79-86.
48. Galli M, Comfurius P, Barbui T, Zwaal RF, Bevers EM. Anticoagulant activity of beta 2-glycoprotein I is potentiated by a distinct subgroup of anticardiolipin antibodies. Thromb Haemost 1992; 68: 297-300.
49. Hunt J, Krilis S. The fifth domain of beta 2-glycoprotein I contains a phospholipid binding site (Cys281-Cys288) and a region recognized by anticardiolipin antibodies. J Immunol 1994; 152: 653-9.
50. George J, Gilburd B, Hojnik M, Levy Y, Langevitz P, Matsuura E, Koike T, Shoenfeld Y. Target recognition of beta2-glycoprotein I (beta2GPI)-dependent anticardiolipin antibodies: evidence for involvement of the fourth domain of beta2GPI in antibody binding. J Immunol 1998; 160: 3917-23.
51. Iverson GM, Victoria EJ, Marquis DM. Anti-beta2 glycoprotein I (beta2GPI) autoantibodies recognize an epitope on the first domain of beta2GPI. Proc Natl Acad Sci USA 1998; 95: 15542-6.
52. McNeeley PA, Dlott JS, Furie RA, Jack RM, Ortel TL, Triplett DA, Victoria EJ, Linnik MD. Beta2-glycoprotein I-dependent anticardiolipin antibodies preferentially bind the amino terminal domain of beta2-glycoprotein I. Thromb Haemost 2001; 86: 590-5.
53. Iverson GM, Matsuura E, Victoria EJ, Cockerill KA, Linnik MD. The orientation of beta-2-GPI on the plate is important for the binding of anti-beta2GPI autoantibodies by elisa. J Autoimmun 2002; 18: 289-97.
54. Horbach DA, van Oort E, Derksen RH, de Groot PG. The contribution of anti-prothrombin-antibodies to lupus anticoagulant activity - discrimination between functional and non-functional anti-prothrombinantibodies. Thromb Haemost 1998; 79: 790-5.
55. Rao LV, Hoang AD, Rapaport SI. Mechanism and effects of the binding of lupus anticoagulant IgG and prothrombin to surface phospholipid. Blood 1996; 88: 4173-82.
56. Simmelink MJ, Horbach DA, Derksen RH, Meijers JC, Bevers EM, Willems GM, De Groot PG. Complexes of anti-prothrombin antibodies and prothrombin cause lupus anticoagulant activity by competing with the binding of clotting factors for catalytic phospholipid surfaces. Br J Haematol 2001; 113: 621-9.
57. Field SL, Chesterman CN, Dai YP, Hogg PJ. Lupus antibody bivalency is required to enhance prothrombin binding to phospholipid. J Immunol 2001; 166: 6118-25.
58. Akimoto T, Akama T, Kono I, Sumida T. Relationship between clinical features and binding domains of anti-prothrombin autoantibodies in patients with systemic lupus erythematosus and antiphospholipid syndrome. Lupus 1999; 8: 761-6.
59. Puurunen M, Manttari M, Manninen V, Palosuo T, Vaarala O. Antibodies to prothrombin crossreact with plasminogen in patients developing myocardial infarction. Br J Haematol 1998; 100: 374-9.
60. Jones DW, Nicholls PJ, Donohoe S, Gallimore MJ, Winter M. Antibodies to factor XII are distinct from antibodies to prothrombin in patients with the anti-phospholipid syndrome. Thromb Haemost 2002; 87: 426-30.
61. Exner T, Kraus M. A monoclonal antibody against prothrombin fragment 1 behaves like a lupus anticoagulant. Thromb Haemost 1999; 81: 470-1.
62. Le Querrec A, Arnout J, Arnoux D, Borg JY, Caron C, Darnige L, Delahousse B, Reber G, Sie P. Quantification of lupus anticoagulants in clinical samples using anti-beta2GP1 and anti-prothrombin monoclonal antibodies. Thromb Haemost 2001; 86: 584-9.
63. Arnout J, Boon D, Vandervoort P, Vanrusselt M, Vermylen J. A monoclonal antibody against prothrombin fragment 2 behaves like a lupus anticoagulant. Lupus 2002; 11: 550.
64. Arnout J. Antiphospholipid syndrome: diagnostic aspects of lupus anticoagulants. Thromb Haemost 2001; 86: 83-91.
65. Horbach DA, van Oort E, Donders RC, Derksen RH, de Groot PG. Lupus anticoagulant is the strongest risk factor for both venous and arterial thrombosis in patients with systemic lupus erythematosus. Comparison between different assays for the detection of antiphospholipid antibodies. Thromb Haemost 1996; 76: 916-24.
66. Wahl DG, Guillemin F, de Maistre E, Perret C, Lecompte T, Thibaut G. Risk for venous thrombosis related to antiphospholipid antibodies in systemic lupus erythematosus - a meta-analysis. Lupus 1997; 6: 467-73.
67. Wahl DG, Guillemin F, de Maistre E, Perret-Guillaume C, Lecompte T, Thibaut G. Meta-analysis of the risk of venous thrombosis in individuals with antiphospholipid antibodies without underlying autoimmune disease or previous thrombosis. Lupus 1998; 7: 15-22.
68. Galli M, Luciani D, Bertolini G, Barbui T. Lupus anticoagulants are stronger risk factors of thrombosis than anticardiolipin antibodies in the antiphospholipid syndrome. A systematic review of the literature. Blood 2003; 101: 1827-32.
69. Bevers EM, Comfurius P, Dekkers DW, Zwaal RF. Lipid translocation across the plasma membrane of mammalian cells. Biochim Biophys Acta 1999; 1439: 317-30.
70. Heemskerk JW, Bevers EM, Lindhout T. Platelet activation and blood coagulation. Thromb Haemost 2002; 88: 186-93.
71. Siljander P, Farndale RW, Feijge MA, Comfurius P, Kos S, Bevers EM, Heemskerk JW. Platelet adhesion enhances the glycoprotein VI-dependent procoagulant response: Involvement of p38 MAP kinase and calpain. Arterioscler Thromb Vasc Biol 2001; 21: 618-27.
72. Rauch U, Bonderman D, Bohrman B, Badimon JJ, Himber J, Riederer MA, Nemerson Y. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood 2000; 96: 170-5.
73. Rosove MH, Brewer PMC. Antiphospholipid thrombosis: Clinical course after the first thrombotic event in 70 patients. Ann Intern Med 1992; 117: 303-8.
74. Khamashta MA, Cuadrado MJ, Mujic F, Taub NA, Hunt BJ, Hughes GR. The management of thrombosis in the antiphospholipid-antibody syndrome. N Engl J Med 1995; 332: 993-7.
75. Esmon CT. Regulation of blood coagulation. Biochim Biophys Acta 2000; 1477: 349-60.
76. Galli M, Ruggeri L, Barbui T. Differential effects of anti-beta2-glycoprotein I and antiprothrombin antibodies on the anticoagulant activity of activated protein C. Blood 1998; 91: 1999-2004.
77. Salemink I, Blezer R, Willems GM, Galli M, Bevers E, Lindhout T. Antibodies to beta2-glycoprotein I associated with antiphospholipid syndrome suppress the inhibitory activity of tissue factor pathway inhibitor. Thromb Haemost 2000; 84: 653-6.
78. Safa O, Hensley K, Smirnov MD, Esmon CT, Esmon NL. Lipid oxidation enhances the function of activated protein C. J Biol Chem 2001; 276: 1829-36.
79. Field SL, Hogg PJ, Daly EB, Dai YP, Murray B, Owens D, Chesterman CN. Lupus anticoagulants form immune complexes with prothrombin and phospholipid that can augment thrombin production in flow. Blood 1999; 94: 3421-31.
80. Arnout J. The pathogenesis of the antiphospholipid syndrome: a hypothesis based on parallelisms with heparin-induced thrombocytopenia. Thromb Haemost 1996; 75: 536-41.
81. Vermylen J, Hoylaerts MF, Arnout J. Antibody-mediated thrombosis. Thromb Haemost 1997; 78: 420-6.
82. Warkentin TE, Chong BH, Greinacher A. Heparin-induced thrombocytopenia: towards consensus. Thromb Haemost 1998; 79: 1-7.
83. Khairy M, Lasne D, Brohard-Bohn B, Aiach M, Rendu F, Bachelot-Loza C. A new approach in the study of the molecular and cellular events implicated in heparin-induced thrombocytopenia. Formation of leukocyte-platelet aggregates. Thromb Haemost 2001; 85: 1090-6.
84. Lutters BC, Meijers JC, Derksen RH, Arnout J, de Groot PG. Dimers of beta 2-glycoprotein I mimic the in vitro effects of beta 2-glycoprotein I-anti-beta 2-glycoprotein I antibody complexes. J Biol Chem 2001; 276: 3060-7.
85. 2-Glycoprotein I. structure and function. Thromb Haemost 2001; (Suppl.): abstractSY925.
86. Jankowski M, Vreys I,Wittevrongel C, Boon D, Vermylen J, Hoylaerts MF, Arnout J. Thrombogenicity of beta-2-glycoprotein I dependent antiphospholipid antibodies in a photochemically induced thrombosis model in the hamster. Blood 2003; 101: 157-62.
87. Pierangeli SS, Liu X, Barker JH, Anderson G, Harris EN. Induction of thrombosis in mouse model by IgG, IgM and IgA immunoglobulins from patients with antiphospholipid syndrome. Thromb Haemost 1995; 74: 1361-7.
88. Hirsh J, Dalen JE, Guyatt G. The sixth (2000) ACCP guidelines for antithrombotic therapy for prevention and treatment of thrombosis. Chest 2001; 119: 1S-2S.
89. Cervera R, Piette JC, Font J, Khamashta MA, Shoenfeld Y, Camps MT, Jacobsen S, Lakos G, Tincani A, Kontopoulou-Griva I, Galeazzi M, Meroni PL, Derksen RH, de Groot PG, Gromnica-Ihle E, Baleva M, Mosca M, Bombardieri S, Houssiau F, Gris JC, Quere I, Hachulla E, Vasconcelos C, Roch B, Fernandez-Nebro A, Boffa MC, Hughes GR, Ingelmo M. Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis Rheum 2002; 46: 1019-27.
90. Lockshin MD. Pregnancy loss and antiphospholipid antibodies. Lupus 1998; 7 (Suppl. 2): S86-S89.
91. Reisner SA, Brenner B, Haim N, Edoute Y, Markiewicz W. Echocardiography in nonbacterial thrombotic endocarditis: from autopsy to clinical entity. J Am Soc Echocardiogr 2000; 13: 876-81.
92. Weenig RH, Davis MDP, Dahl PR, Su WPD. Skin ulcers misdiagnosed as pyoderma gangrenosum. N Engl J Med 2002; 347: 1412-8.
93. Petri M, Rheinschmidt M, Whiting-O'Keefe Q, Hellmann D, Corash L. The frequency of lupus anticoagulant in systemic lupus erythematosus. A study of sixty consecutive patients by activated partial thromboplastin time, Russell viper venom time, and anticardiolipin antibody level. Ann Intern Med 1987; 106: 524-31.
94. Galli M, Finazzi G, Norbis F, Marziali S, Marchioli R, Barbui T. The risk of thrombosis in patients with lupus anticoagulants is predicted by their specific coagulation profile. Thromb Haemost 1999; 81: 695-700.
95. Galli M, Dlott J, Norbis F, Ruggeri L, Cler L, Triplett DA, Barbui T. Lupus anticoagulants and thrombosis: clinical association of different coagulation and immunologic tests. Thromb Haemost 2000; 84: 1012-6.
96. 2glycoprotein I- and prothrombindependent lupus anticoagulants. Thromb Haemost 2003; 89: in press.
97. Harris EN, Pierangeli SS. Revisiting the anticardiolipin test and its standardization. Lupus 2002; 11: 269-75.
98. Hunt JE, McNeil HP, Morgan GJ, Crameri RM, Krilis SA. A phospholipid-beta 2-glycoprotein I complex is an antigen for anticardiolipin antibodies occurring in autoimmune disease but not with infection. Lupus 1992; 1: 75-81.
99. Reber G, Arvieux J, Comby E, Degenne D, de Moerloose P, Sanmarco M, Potron G. Multicenter evaluation of nine commercial kits for the quantitation of anticardiolipin antibodies. The Working Group on Methodologies in Haemostasis from the GEHT (Groupe d'Etudes sur l'Hemostase et la Thrombose). Thromb Haemost 1995; 73: 444-52.
100. Tincani A, Allegri F, Sanmarco M, Cinquini M, Taglietti M, Balestrieri G, Koike T, Ichikawa K, Meroni P, Boffa MC. Anticardiolipin antibody assay: a methodological analysis for a better consensus in routine determinations. A cooperative project of the European Antiphospholipid Forum. Thromb Haemost 2001; 86: 575-83.
101. Audrain MA, El-Kouri D, Hamidou MA, Mioche L, Ibara A, Langlois ML, Muller JY. Value of autoantibodies to beta(2)-glycoprotein 1 in the diagnosis of antiphospholipid syndrome. Rheumatology (Oxford) 2002; 41: 550-3.
102. Galli M, Barbui T. Antiprothrombin antibodies: detection and clinical significance in the antiphospholipid syndrome. Blood 1999; 93: 2149-57.
103. Reber G, Schousboe I, Tincani A, Sanmarco M, Kveder T, de Moerloose P, Boffa MC, Arvieux J. Inter-laboratory variability of antibeta2-glycoprotein I measurement. A collaborative study in the frame of the European Forum on Antiphospholipid Antibodies Standardization Group. Thromb Haemost 2002; 88: 66-73.
104. Brighton TA, Dai YP, Hogg PJ, Chesterman CN. Microheterogeneity of beta-2 glycoprotein I. implications for binding to anionic phospholipids. Biochem J 1999; 340: 59-67.
105. Hyers TM, Agnelli G, Hull RD, Morris TA, Samama M, TapsonV,Weg JG. Antithrombotic therapy for venous thromboembolic disease. Chest 2001; 119 (Suppl. 1): 176S-193S.
106. Derksen RHWM, de Groot PhG, Kater L, Nieuwenhuis HK. Patients with antiphospholipid antibodies and venous thrombosis should receive long term anticoagulant treatment. Ann Rheum Dis 1993; 52: 689-92.
107. Derksen RH, de Groot PG. Do we know which patients with the antiphospholipid syndrome should receive long-term high dose anticoagulation? J Autoimmun 2000; 15: 255-9.
108. Ginsberg JS, Wells PS, Brill-Edwards P, Donovan D, Moffatt K, Johnston M, Stevens P, Hirsh J. Antiphospholipid antibodies and venous thromboembolism. Blood 1995; 86: 3685-91.
109. Schulman S, Svenungsson E, Granqvist S. Anticardiolipin antibodies predict early recurrence of thromboembolism and death among patients with venous thromboembolism following anticoagulant therapy. Duration Anticoagulation Study Group. Am J Med 1998; 104: 332-8.
110. Douketis JD, Crowther MA, Julian JA, Stewart K, Donovan D, Kaminska EA, Laskin CA, Ginsberg JS. The effects of low-intensity warfarin on coagulation activation in patients with antiphospholipid antibodies and systemic lupus erythematosus. Thromb Haemost 1999; 82: 1028-32.
111. Finazzi G, Barbui T. Feasibility of a randomized clinical trial for the prevention of recurrent thrombosis in the antiphospholipid syndrome: the WAPS project. Provisional Steering Committee of the Warfarin in Antiphospholipid Syndrome (WAPS) Study. Ann Med Interne 1996; 147: 38-41.
112. De Cuypere E, Peerlinck K, Verhaeghe R, Vanrusselt M, Arnout J, Vermylen J. A vitamin K antagonist rapidly reverses a blue toe syndrome in a patient with lupus anticoagulant and antiprothrombin antibodies. Acta Clin Belg 2002; 57: 74-8.
113. Vivaldi P, Rossetti G, Galli M, Finazzi G. Severe bleeding due to acquired hypoprothrombinemia-lupus anticoagulant syndrome. Case report and review of literature. Haematologica 1997; 82: 345-7.
114. Ginsberg JS, Greer I, Hirsh J. Use of antithrombotic agents during pregnancy. Chest 2001; 119 (Suppl. 1): 122S-131S.
115. Guerin J, Sheng Y, Reddel S, Iverson GM, Chapman MG, Krilis SA. Heparin inhibits the binding of beta 2-glycoprotein I to phospholipids and promotes the plasmin-mediated inactivation of this blood protein. Elucidation of the consequences of the two biological events in patients with the anti-phospholipid syndrome. J Biol Chem 2002; 277: 2644-9.